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Cellular basis of tissue regeneration by omentum.

Shah S, Lowery E, Braun RK, Martin A, Huang N, Medina M, Sethupathi P, Seki Y, Takami M, Byrne K, Wigfield C, Love RB, Iwashima M - PLoS ONE (2012)

Bottom Line: To understand the mechanism of tissue repair support by the omentum in more detail, we analyzed the cell subsets derived from the omentum on immune and inflammatory responses.Our data demonstrate that the omentum contains at least two groups of cells that support tissue repair, immunomodulatory myeloid derived suppressor cells and omnipotent stem cells that are indistinguishable from mesenchymal stem cells.Based on these data, we propose that the omentum is a designated organ for tissue repair and healing in response to foreign invasion and tissue damage.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology and Immunology, Stritch School of Medicine, Loyola University Chicago, Chicago, Illinois, United States of America.

ABSTRACT
The omentum is a sheet-like tissue attached to the greater curvature of the stomach and contains secondary lymphoid organs called milky spots. The omentum has been used for its healing potential for over 100 years by transposing the omental pedicle to injured organs (omental transposition), but the mechanism by which omentum helps the healing process of damaged tissues is not well understood. Omental transposition promotes expansion of pancreatic islets, hepatocytes, embryonic kidney, and neurons. Omental cells (OCs) can be activated by foreign bodies in vivo. Once activated, they become a rich source for growth factors and express pluripotent stem cell markers. Moreover, OCs become engrafted in injured tissues suggesting that they might function as stem cells.Omentum consists of a variety of phenotypically and functionally distinctive cells. To understand the mechanism of tissue repair support by the omentum in more detail, we analyzed the cell subsets derived from the omentum on immune and inflammatory responses. Our data demonstrate that the omentum contains at least two groups of cells that support tissue repair, immunomodulatory myeloid derived suppressor cells and omnipotent stem cells that are indistinguishable from mesenchymal stem cells. Based on these data, we propose that the omentum is a designated organ for tissue repair and healing in response to foreign invasion and tissue damage.

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Effect of omentum cells on ex vivo T cell proliferation.(a) CFSE labeled splenocytes were cultured with or without omentum cells in a 1∶1 ratio for 3 days. T cells were either left unstimulated (grey solid) or stimulated with 1 µg/ml anti-CD3 (dark lines). Cells were labeled with anti-CD4 and analyzed by flow cytometry. (b) Surface phenotypic analysis of cells derived from naïve and day 7 omentum by flow cytometry. (c) Omentum cells were sorted into CD45− and CD45+ cells before culturing with CFSE labeled splenocytes with 1 µg/ml anti-CD3 (solid lines) or left unstimulated (dotted lines). Cells were harvested and surface labeled with anti-CD4. (d) Surface antigen expression by CD45+ omentum cells: Activated omentum cells were stained and analyzed for the expression of antigens indicated. (e) iNOS expression was determined in total omentum cells, CD45+ omentum cells, or CD45− omentum cells upon IFNγ stimulation for 24 hrs by western blotting. (f) Omentum cells were sorted into Gr1+/Gr1− cells and tested as in (c) for the effect on T cell proliferation.
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pone-0038368-g003: Effect of omentum cells on ex vivo T cell proliferation.(a) CFSE labeled splenocytes were cultured with or without omentum cells in a 1∶1 ratio for 3 days. T cells were either left unstimulated (grey solid) or stimulated with 1 µg/ml anti-CD3 (dark lines). Cells were labeled with anti-CD4 and analyzed by flow cytometry. (b) Surface phenotypic analysis of cells derived from naïve and day 7 omentum by flow cytometry. (c) Omentum cells were sorted into CD45− and CD45+ cells before culturing with CFSE labeled splenocytes with 1 µg/ml anti-CD3 (solid lines) or left unstimulated (dotted lines). Cells were harvested and surface labeled with anti-CD4. (d) Surface antigen expression by CD45+ omentum cells: Activated omentum cells were stained and analyzed for the expression of antigens indicated. (e) iNOS expression was determined in total omentum cells, CD45+ omentum cells, or CD45− omentum cells upon IFNγ stimulation for 24 hrs by western blotting. (f) Omentum cells were sorted into Gr1+/Gr1− cells and tested as in (c) for the effect on T cell proliferation.

Mentions: T cells play critical roles in inflammation and following fibrosis in the bleomycin-induced tissue injury models [28]–[30]. To elucidate the mechanism by which omentum cells helped healing of the lung, we determined if omentum cells suppress T cell proliferation and function. CFSE labeled splenocytes were stimulated by anti-CD3 antibody to induce proliferation in the presence or absence of omentum cells. After 3 days, the proliferation of CD4+ and CD8+ T cells was dramatically reduced in the presence of omentum cells (Fig. 2a and Fig. 3a). Inhibition of T cell proliferation was observed when omentum cells were added as low as 1/10 of splenocytes and correlated to the omentum cell numbers added to the culture (omentum∶splenocytes ratios ranged from 1∶10∼1∶1) (Fig. 2a). Inhibition of cell proliferation was not due to the deterioration of culture conditions since addition of the same number of suspended lung cells had no effect on T cell proliferation (Fig. 2b). Further, inhibition of T cell proliferation by omentum cells was not observed when cells were separated in a transwell culture system (Fig. 2c) suggesting that cell-cell contact or locally acting factors are important for T cell suppression.


Cellular basis of tissue regeneration by omentum.

Shah S, Lowery E, Braun RK, Martin A, Huang N, Medina M, Sethupathi P, Seki Y, Takami M, Byrne K, Wigfield C, Love RB, Iwashima M - PLoS ONE (2012)

Effect of omentum cells on ex vivo T cell proliferation.(a) CFSE labeled splenocytes were cultured with or without omentum cells in a 1∶1 ratio for 3 days. T cells were either left unstimulated (grey solid) or stimulated with 1 µg/ml anti-CD3 (dark lines). Cells were labeled with anti-CD4 and analyzed by flow cytometry. (b) Surface phenotypic analysis of cells derived from naïve and day 7 omentum by flow cytometry. (c) Omentum cells were sorted into CD45− and CD45+ cells before culturing with CFSE labeled splenocytes with 1 µg/ml anti-CD3 (solid lines) or left unstimulated (dotted lines). Cells were harvested and surface labeled with anti-CD4. (d) Surface antigen expression by CD45+ omentum cells: Activated omentum cells were stained and analyzed for the expression of antigens indicated. (e) iNOS expression was determined in total omentum cells, CD45+ omentum cells, or CD45− omentum cells upon IFNγ stimulation for 24 hrs by western blotting. (f) Omentum cells were sorted into Gr1+/Gr1− cells and tested as in (c) for the effect on T cell proliferation.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3368844&req=5

pone-0038368-g003: Effect of omentum cells on ex vivo T cell proliferation.(a) CFSE labeled splenocytes were cultured with or without omentum cells in a 1∶1 ratio for 3 days. T cells were either left unstimulated (grey solid) or stimulated with 1 µg/ml anti-CD3 (dark lines). Cells were labeled with anti-CD4 and analyzed by flow cytometry. (b) Surface phenotypic analysis of cells derived from naïve and day 7 omentum by flow cytometry. (c) Omentum cells were sorted into CD45− and CD45+ cells before culturing with CFSE labeled splenocytes with 1 µg/ml anti-CD3 (solid lines) or left unstimulated (dotted lines). Cells were harvested and surface labeled with anti-CD4. (d) Surface antigen expression by CD45+ omentum cells: Activated omentum cells were stained and analyzed for the expression of antigens indicated. (e) iNOS expression was determined in total omentum cells, CD45+ omentum cells, or CD45− omentum cells upon IFNγ stimulation for 24 hrs by western blotting. (f) Omentum cells were sorted into Gr1+/Gr1− cells and tested as in (c) for the effect on T cell proliferation.
Mentions: T cells play critical roles in inflammation and following fibrosis in the bleomycin-induced tissue injury models [28]–[30]. To elucidate the mechanism by which omentum cells helped healing of the lung, we determined if omentum cells suppress T cell proliferation and function. CFSE labeled splenocytes were stimulated by anti-CD3 antibody to induce proliferation in the presence or absence of omentum cells. After 3 days, the proliferation of CD4+ and CD8+ T cells was dramatically reduced in the presence of omentum cells (Fig. 2a and Fig. 3a). Inhibition of T cell proliferation was observed when omentum cells were added as low as 1/10 of splenocytes and correlated to the omentum cell numbers added to the culture (omentum∶splenocytes ratios ranged from 1∶10∼1∶1) (Fig. 2a). Inhibition of cell proliferation was not due to the deterioration of culture conditions since addition of the same number of suspended lung cells had no effect on T cell proliferation (Fig. 2b). Further, inhibition of T cell proliferation by omentum cells was not observed when cells were separated in a transwell culture system (Fig. 2c) suggesting that cell-cell contact or locally acting factors are important for T cell suppression.

Bottom Line: To understand the mechanism of tissue repair support by the omentum in more detail, we analyzed the cell subsets derived from the omentum on immune and inflammatory responses.Our data demonstrate that the omentum contains at least two groups of cells that support tissue repair, immunomodulatory myeloid derived suppressor cells and omnipotent stem cells that are indistinguishable from mesenchymal stem cells.Based on these data, we propose that the omentum is a designated organ for tissue repair and healing in response to foreign invasion and tissue damage.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology and Immunology, Stritch School of Medicine, Loyola University Chicago, Chicago, Illinois, United States of America.

ABSTRACT
The omentum is a sheet-like tissue attached to the greater curvature of the stomach and contains secondary lymphoid organs called milky spots. The omentum has been used for its healing potential for over 100 years by transposing the omental pedicle to injured organs (omental transposition), but the mechanism by which omentum helps the healing process of damaged tissues is not well understood. Omental transposition promotes expansion of pancreatic islets, hepatocytes, embryonic kidney, and neurons. Omental cells (OCs) can be activated by foreign bodies in vivo. Once activated, they become a rich source for growth factors and express pluripotent stem cell markers. Moreover, OCs become engrafted in injured tissues suggesting that they might function as stem cells.Omentum consists of a variety of phenotypically and functionally distinctive cells. To understand the mechanism of tissue repair support by the omentum in more detail, we analyzed the cell subsets derived from the omentum on immune and inflammatory responses. Our data demonstrate that the omentum contains at least two groups of cells that support tissue repair, immunomodulatory myeloid derived suppressor cells and omnipotent stem cells that are indistinguishable from mesenchymal stem cells. Based on these data, we propose that the omentum is a designated organ for tissue repair and healing in response to foreign invasion and tissue damage.

Show MeSH
Related in: MedlinePlus